A massive Kilrathi armada attacks a remote human base and captures a navigation computer, through which it will be able to locate Earth. Admiral Tolwyn (David Warner) directs Blair, whose parents he knew, to carry orders to the Tiger Claw to fight a suicidal delaying action to let the rest of the Terran fleet reach Earth. Along with the awkwardness of joining a new unit, and continual pranks that require discipline from wing commander Deveraux (Saffron Burrows), Blair fights the distrust of his crewmates because of the drastic orders he brings from the Admiral, and because his mother was a "Pilgrim", a strain of humans who had fought against the Confederation. Pilgrims have the innate ability to navigate space by feel despite obstacles such as black holes. Marshall falls in love with Lieutenant Rosie Forbes (Ginny Holder) but she dies when the two disobey orders and engage Kilrathi fighters.

Tiger Claw personnel successfully attack and destroy the Kilrathi command ship. In the attack, they also find the stolen navigation computer and learn the space-jump the Kilrathi fleet will use to approach Earth. The Tiger Claw, however, is disabled and can do nothing more to prevent the assault, except to send Deveraux and Blair in fighters to find their way back to Earth. If alerted to the Kilrathi's plans, Earth forces can destroy each Kilrathi ship before it can get its bearings after the space-jump; if not, Earth will surely be overwhelmed.

Deveraux's fighter is disabled in combat, but she convinces Blair to abandon her and continue his mission. Blair uses his Pilgrim ability to make the jump to the vicinity of Earth. He is followed by a Kilrathi ship, but he locates a black hole he encountered at the start of the movie and induces the Kilrathi ship to venture so close as to be devoured by it. As his fighter runs out of fuel, he transmits the information Earth needs to defeat the Kilrathi assault. The Earth fleet rescues Blair, and Taggart rescues Deveraux.

The film has been criticized by some fans for altering the visual style of the most recent Wing Commander games. The most notable shift between the games and the movie is the appearance of the Kilrathi. Although the movie's Kilrathi retain feline facial characteristics, they lose their signature fur entirely. Roberts has since said that this change was a result of his ongoing unhappiness with the appearance of the 'live' Kilrathi, none of which lived up to his internal vision. He had previously re-imagined the Kilrathi between Wing Commander III and IV, going so far as to completely redesign the Melek character between the two games.[1][2] Roberts, even after production of the film, was left unsatisfied with the results of the film version of the Kilrathi;[3] some interviews imply that the puppets were built before the sets were completed, and were too large to be filmed without hunching over unnaturally.

Several changes in character backgrounds and nationalities were also made, as well as plot and name changes. The 'pilgrim' story is new to the film, although there is some resemblance to the borderworlders of Wing Commander IV. The carrier's name was changed to Tiger Claw, rather than Tiger's Claw. The visual appearance of the ships also changed radically; the Rapier fighters featured in the film were built from scrapped English Electric Lightning jet fighter fuselages.

Roberts cast actors that bore little physical resemblance to those who previously held the part. However, this was not the first time characters' appearances got an overhaul. Paladin, for example, has gone from being a thin fair-haired man in Wing Commander I & II[4] (voiced by Martin Davies) to being a large dark-haired Scotsman in Wing Commander III and IV[5] (played by John Rhys-Davies) to have a French accent in the movie[6] (played by Karyo).

Wing Commander Arena, the latest game in the series, makes reference to the movie, including references to the Pilgrim War,[7] while using ships and settings which first appeared in the main series of games.[8]

The novelization of the film by Peter Telep was fairly faithful to the film itself. However, in the book the plot to discredit Blair is more far-reaching and includes David Suchet's character, Captain Jason Sansky. There is also more general information about the Kilrathi and their first attack on a space station. The novel is based on the film's shooting script, which includes most of this information. Significant cuts removed the 'traitor' subplot from the finished film, since it heavily involved the unimpressive Kilrathi puppets. Admiral Bill Wilson was to be the traitor that compromised the Pegasus station (there were a number of scenes between Wilson and Bokoth, the commander of the Kilrathi battle group). In addition, Wilson provoked a knife fight on board the Kilrathi ConCom between Blair and Commander Gerald. Gerald wounded Blair, but everyone came to their senses and Blair used his Pilgrim Cross knife to kill Admiral Wilson (the only surviving element of this in the film is that Blair has a bandage on his hand during the scene where Paladin gave Blair his Pilgrim Cross). Also, Sansky was to commit suicide rather than be captured as a traitor; however, since all of his 'traitor' scenes were removed, the film now implies that Sansky died from head injuries he received during battle.